Supplementary eye field activity reflects a decision rule governing smooth pursuit but not the decision

Animals depend on learned rules to guide their actions. Prefrontal (PFC) and premotor (PMC) cortex of primates have been reported to display rule-related neural activity, but it is unclear how signals encoded here are utilized to enforce the decision to act. The supplementary eye field (SEF) is a candidate for enforcing rule-guided ocular decisions because the activity of neurons here is correlated with the rule in an ocular decision-making task and because this area is anatomically more proximal to movement structures than PFC and PMC and receives inputs from them. However, in the previous work, the rule encoding and ocular outcome were confounded, leaving open the question of whether SEF activity is related to the rule or the behavior. In the present study, we attempted to discriminate between these alternatives by increasing task difficulty and forcing errors, thereby putting the stimulus and the behavior at odds. Single SEF neurons were recorded while monkeys performed the task in which the rule is to pursue a moving target if it intersects a visible square and maintain fixation if it does not. A delay period was imposed to monitor neural activity while the target approached the square. Two complementary populations of go and nogo neurons were found. When task difficulty was increased, the monkeys made more errors, and the neurons took longer to encode the rule. However, in error trials, most neurons continued to reflect the rule rather the monkey's ocular decision in both the delay period and after square intersection (movement period). This was the case for both directionally tuned and nondirectional SEF neurons. The results suggest that SEF neurons encode the ocular decision rule but that the decision itself likely occurs in a different structure that sums rule information from the SEF with information from other areas.